skip to main content


Title: Genomic Variation Influences Methanothermococcus Fitness in Marine Hydrothermal Systems
Hydrogenotrophic methanogens are ubiquitous chemoautotrophic archaea inhabiting globally distributed deep-sea hydrothermal vent ecosystems and associated subseafloor niches within the rocky subseafloor, yet little is known about how they adapt and diversify in these habitats. To determine genomic variation and selection pressure within methanogenic populations at vents, we examined five Methanothermococcus single cell amplified genomes (SAGs) in conjunction with 15 metagenomes and 10 metatranscriptomes from venting fluids at two geochemically distinct hydrothermal vent fields on the Mid-Cayman Rise in the Caribbean Sea. We observed that some Methanothermococcus lineages and their transcripts were more abundant than others in individual vent sites, indicating differential fitness among lineages. The relative abundances of lineages represented by SAGs in each of the samples matched phylogenetic relationships based on single-copy universal genes, and genes related to nitrogen fixation and the CRISPR/Cas immune system were among those differentiating the clades. Lineages possessing these genes were less abundant than those missing that genomic region. Overall, patterns in nucleotide variation indicated that the population dynamics of Methanothermococcus were not governed by clonal expansions or selective sweeps, at least in the habitats and sampling times included in this study. Together, our results show that although specific lineages of Methanothermococcus co-exist in these habitats, some outcompete others, and possession of accessory metabolic functions does not necessarily provide a fitness advantage in these habitats in all conditions. This work highlights the power of combining single-cell, metagenomic, and metatranscriptomic datasets to determine how evolution shapes microbial abundance and diversity in hydrothermal vent ecosystems.  more » « less
Award ID(s):
1826734
NSF-PAR ID:
10325466
Author(s) / Creator(s):
; ; ; ; ;
Date Published:
Journal Name:
Frontiers in Microbiology
Volume:
12
ISSN:
1664-302X
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ABSTRACT Chloroflexi small-subunit (SSU) rRNA gene sequences are frequently recovered from subseafloor environments, but the metabolic potential of the phylum is poorly understood. The phylum Chloroflexi is represented by isolates with diverse metabolic strategies, including anoxic phototrophy, fermentation, and reductive dehalogenation; therefore, function cannot be attributed to these organisms based solely on phylogeny. Single-cell genomics can provide metabolic insights into uncultured organisms, like the deep-subsurface Chloroflexi . Nine SSU rRNA gene sequences were identified from single-cell sorts of whole-round core material collected from the Okinawa Trough at Iheya North hydrothermal field as part of Integrated Ocean Drilling Program (IODP) expedition 331 (Deep Hot Biosphere). Previous studies of subsurface Chloroflexi single amplified genomes (SAGs) suggested heterotrophic or lithotrophic metabolisms and provided no evidence for growth by reductive dehalogenation. Our nine Chloroflexi SAGs (seven of which are from the order Anaerolineales ) indicate that, in addition to genes for the Wood-Ljungdahl pathway, exogenous carbon sources can be actively transported into cells. At least one subunit for pyruvate ferredoxin oxidoreductase was found in four of the Chloroflexi SAGs. This protein can provide a link between the Wood-Ljungdahl pathway and other carbon anabolic pathways. Finally, one of the seven Anaerolineales SAGs contains a distinct reductive dehalogenase homologous ( rdhA ) gene. IMPORTANCE Through the use of single amplified genomes (SAGs), we have extended the metabolic potential of an understudied group of subsurface microbes, the Chloroflexi . These microbes are frequently detected in the subsurface biosphere, though their metabolic capabilities have remained elusive. In contrast to previously examined Chloroflexi SAGs, our genomes (several are from the order Anaerolineales ) were recovered from a hydrothermally driven system and therefore provide a unique window into the metabolic potential of this type of habitat. In addition, a reductive dehalogenase gene ( rdhA ) has been directly linked to marine subsurface Chloroflexi , suggesting that reductive dehalogenation is not limited to the class Dehalococcoidia . This discovery expands the nutrient-cycling and metabolic potential present within the deep subsurface and provides functional gene information relating to this enigmatic group. 
    more » « less
  2. Summary

    Elucidation of the potential roles of single‐celled eukaryotes (protists) in ecosystem function and trophodynamics in hydrothermal vent ecosystems is reliant on information regarding their abundance, distribution and preference for vent habitats. Using high‐throughput 18S rRNA gene sequencing on a diverse suite of hydrothermally influenced and background water samples, we assess the diversity and distribution of protists and identify potential vent endemics. We found that 95% of the recovered sequences belong to operational taxonomic units (OTUs) with a cosmopolitan distribution across vent and non‐vent habitats. Analysis of ‘vent only’ OTUs found in more than one vent sample and co‐occurrence network analysis comparing protist groups to extremophilic reference organisms suggest that the most likely vent endemics are infrequently encountered, potentially in low abundance, and belong to novel lineages, both at the phylum level and within defined clades of Rhizaria and Stramenopila. Potential endemism is inferred for relatives of known apusomonads, excavates and some clades of Syndiniales. Similarity in community composition among samples was low, indicating a strong stochastic component to protist community assembly and suggesting that rare endemics may serve as a reservoir poised to respond to changing environmental conditions in these dynamic systems.

     
    more » « less
  3. Abstract

    Chemosynthetic animal-microbe symbioses sustain hydrothermal vent communities in the global deep sea. In the Indo-Pacific Ocean, hydrothermal ecosystems are often dominated by gastropod species of the genus Alviniconcha, which live in association with chemosynthetic Gammaproteobacteria or Campylobacteria. While the symbiont genomes of most extant Alviniconcha species have been sequenced, no genome information is currently available for the gammaproteobacterial endosymbiont of Alviniconcha adamantis—a comparatively shallow living species that is thought to be the ancestor to all other present Alviniconcha lineages. Here, we report the first genome sequence for the symbiont of A. adamantis from the Chamorro Seamount at the Mariana Arc. Our phylogenomic analyses show that the A. adamantis symbiont is most closely related to Chromatiaceae endosymbionts of the hydrothermal vent snails Alviniconcha strummeri and Chrysomallon squamiferum, but represents a distinct bacterial species or possibly genus. Overall, the functional capacity of the A. adamantis symbiont appeared to be similar to other chemosynthetic Gammaproteobacteria, though several flagella and chemotaxis genes were detected, which are absent in other gammaproteobacterial Alviniconcha symbionts. These differences might suggest potential contrasts in symbiont transmission dynamics, host recognition, or nutrient transfer. Furthermore, an abundance of genes for ammonia transport and urea usage could indicate adaptations to the oligotrophic waters of the Mariana region, possibly via recycling of host- and environment-derived nitrogenous waste products. This genome assembly adds to the growing genomic resources for chemosynthetic bacteria from hydrothermal vents and will be valuable for future comparative genomic analyses assessing gene content evolution in relation to environment and symbiotic lifestyles.

     
    more » « less
  4. null (Ed.)
    The Chicxulub impact crater, on the Yucatán Peninsula of México, is unique. It is the only known terrestrial impact structure that has been directly linked to a mass extinction event and the only terrestrial impact with a global ejecta layer. Of the three largest impact structures on Earth, Chicxulub is the best preserved. Chicxulub is also the only known terrestrial impact structure with an intact, unequivocal topographic peak ring. Chicxulub’s role in the Cretaceous/Paleogene (K-Pg) mass extinction and its exceptional state of preservation make it an important natural laboratory for the study of both large impact crater formation on Earth and other planets and the effects of large impacts on the Earth’s environment and ecology. Our understanding of the impact process is far from complete, and despite more than 30 years of intense debate, we are still striving to answer the question as to why this impact was so catastrophic. During International Ocean Discovery Program (IODP) and International Continental Scientific Drilling Program (ICDP) Expedition 364, Paleogene sedimentary rocks and lithologies that make up the Chicxulub peak ring were cored to investigate (1) the nature and formational mechanism of peak rings, (2) how rocks are weakened during large impacts, (3) the nature and extent of post-impact hydrothermal circulation, (4) the deep biosphere and habitability of the peak ring, and (5) the recovery of life in a sterile zone. Other key targets included sampling the transition through a rare midlatitude Paleogene sedimentary succession that might include Eocene and Paleocene hyperthermals and/or the Paleocene/Eocene Thermal Maximum (PETM); the composition and character of suevite, impact melt rock, and basement rocks in the peak ring; the sedimentology and stratigraphy of the Paleocene–Eocene Chicxulub impact basin infill; the geo- and thermochronology of the rocks forming the peak ring; and any observations from the core that may help constrain the volume of dust and climatically active gases released into the stratosphere by this impact. Petrophysical properties measurements on the core and wireline logs acquired during Expedition 364 will be used to calibrate geophysical models, including seismic reflection and potential field data, and the integration of all the data will calibrate models for impact crater formation and environmental effects. The drilling directly contributes to IODP Science Plan goals: Climate and Ocean Change: How does Earth’s climate system respond to elevated levels of atmospheric CO2? How resilient is the ocean to chemical perturbations? The Chicxulub impact represents an external forcing event that caused a 75% species level mass extinction. The impact basin may also record key hyperthermals within the Paleogene. Biosphere Frontiers: What are the origin, composition, and global significance of subseafloor communities? What are the limits of life in the subseafloor? How sensitive are ecosystems and biodiversity to environmental change? Impact craters can create habitats for subsurface life, and Chicxulub may provide information on potential habitats for life, including extremophiles, on the early Earth and other planetary bodies. Paleontological and geochemical studies at ground zero will document how large impacts affect ecosystems and biodiversity. Earth Connections/Earth in Motion: What mechanisms control the occurrence of destructive earthquakes, landslides, and tsunami? Drilling into the uplifted rocks that form the peak ring will be used to groundtruth numerical simulations and model impact-generated tsunami, and deposits on top of the peak ring and around the Gulf of México will inform us about earthquakes, landslides, and tsunami generated by Chicxulub. These data will collectively help us understand how impact processes are recorded in the geologic record and their potential hazards. IODP Expedition 364 was a Mission Specific Platform expedition designed to obtain subseabed samples and downhole logging measurements from the post-impact sedimentary succession and the peak ring of the Chicxulub impact crater. A single borehole (Hole M0077A) was drilled into the Chicxulub impact crater on the Yucatán continental shelf, recovering core from 505.70 to 1334.69 meters below seafloor (mbsf) with ~99% core recovery. Downhole logs were acquired for the entire depth of the borehole. 
    more » « less
  5. null (Ed.)
    The Chicxulub impact crater, México, is unique. It is the only known terrestrial impact structure that has been directly linked to a mass extinction event and the only terrestrial impact with a global ejecta layer. Of the three largest impact structures on Earth, Chicxulub is the best preserved. Chicxulub is also the only known terrestrial impact structure with an intact, unequivocal topographic peak ring. Chicxulub’s role in the Cretaceous/Paleogene (K-Pg) mass extinction and its exceptional state of preservation make it an important natural laboratory for the study of both large impact crater formation on Earth and other planets and the effects of large impacts on the Earth’s environment and ecology. Our understanding of the impact process is far from complete, and despite more than 30 years of intense debate, we are still striving to answer the question as to why this impact was so catastrophic. During International Ocean Discovery Program (IODP) Expedition 364, Paleogene sediments and lithologies that make up the Chicxulub peak ring were cored to investigate (1) the nature and formational mechanism of peak rings, (2) how rocks are weakened during large impacts, (3) the nature and extent of post-impact hydrothermal circulation, (4) the deep biosphere and habitability of the peak ring, and (5) the recovery of life in a sterile zone. Other key targets included sampling the transition through a rare midlatitude section that might include Eocene and Paleocene hyperthermals and/or the Paleocene/Eocene Thermal Maximum (PETM); the composition and character of the impact breccias, melt rocks, and peak-ring rocks; the sedimentology and stratigraphy of the Paleocene–Eocene Chicxulub impact basin infill; the chronology of the peak-ring rocks; and any observations from the core that may help us constrain the volume of dust and climatically active gases released into the stratosphere by this impact. Petrophysical property measurements on the core and wireline logs acquired during Expedition 364 will be used to calibrate geophysical models, including seismic reflection and potential field data, and the integration of all the data will calibrate impact crater models for crater formation and environmental effects. The proposed drilling directly contributes to IODP Science Plan goals: Climate and Ocean Change: How resilient is the ocean to chemical perturbations? The Chicxulub impact represents an external forcing event that caused a 75% level mass extinction. The impact basin may also record key hyperthermals within the Paleogene. Biosphere Frontiers: What are the origin, composition, and global significance of subseafloor communities? What are the limits of life in the subseafloor? How sensitive are ecosystems and biodiversity to environmental change? Impact craters can create habitats for subsurface life, and Chicxulub may provide information on potential habitats for life, including extremophiles, on the early Earth and other planetary bodies. Paleontological and geochemical studies at ground zero will document how large impacts affect ecosystems and effects on biodiversity. Earth Connections/Earth in Motion: What are the composition, structure and dynamics of Earth’s upper mantle? What mechanisms control the occurrence of destructive earthquakes, landslides, and tsunami? Mantle uplift in response to impacts provides insight into dynamics that differ between Earth and other rocky planets. Impacts generate earthquakes, landslides, and tsunami, and scales that generally exceed plate tectonic processes yield insight into effects, the geologic record, and potential hazards. IODP Expedition 364 was a Mission Specific Platform expedition to obtain subseabed samples and downhole logging measurements from the sedimentary cover sequence and peak ring of the Chicxulub impact crater. A single borehole was drilled into the Chicxulub impact crater on the Yucatán continental shelf, recovering core from 505.7 to 1334.73 m below seafloor with ~99% core recovery and acquiring downhole logs for the entire depth. 
    more » « less